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Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps.

ABSTRACT: We provide the first detailed identification of Barents Sea cold seep frenulate hosts and their symbionts. Mitochondrial COI sequence analysis, in combination with detailed morphological investigations through both light and electron microscopy was used for identifying frenulate hosts, and comparing them to Oligobrachia haakonmosbiensis and Oligobrachia webbi, two morphologically similar species known from the Norwegian Sea. Specimens from sites previously assumed to host O. haakonmosbiensis were included in our molecular analysis, which allowed us to provide new insight on the debate regarding species identity of these Oligobrachia worms. Our results indicate that high Arctic seeps are inhabited by a species that though closely related to Oligobrachia haakonmosbiensis, is nonetheless distinct. We refer to this group as the Oligobrachia sp. CPL-clade, based on the colloquial names of the sites they are currently known to inhabit. Since members of the Oligobrachia sp. CPL-clade cannot be distinguished from O. haakonmosbiensis or O. webbi based on morphology, we suggest that a complex of cryptic Oligobrachia species inhabit seeps in the Norwegian Sea and the Arctic. The symbionts of the Oligobrachia sp. CPL-clade were also found to be closely related to O. haakonmosbiensis symbionts, but genetically distinct. Fluorescent in situ hybridization and transmission electron micrographs revealed extremely dense populations of bacteria within the trophosome of members of the Oligobrachia sp. CPL-clade, which is unusual for frenulates. Bacterial genes for sulfur oxidation were detected and small rod shaped bacteria (round in cross section), typical of siboglinid-associated sulfur-oxidizing bacteria, were seen on electron micrographs of trophosome bacteriocytes, suggesting that sulfide constitutes the main energy source. We hypothesize that specific, local geochemical conditions, in particular, high sulfide fluxes and concentrations could account for the unusually high symbiont densities in members of the Oligrobrachia sp. CPL-clade.

SUBMITTER: Sen A

PROVIDER: S-EPMC6310283 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Frenulate species were identified from a high Arctic methane seep area on Vestnesa Ridge, western Svalbard margin (79°N, Fram Strait) based on mitochondrial cytochrome oxidase subunit I (mtCOI). Two species were found: Oligobrachia haakonmosbiensis, and a new, distinct, and undescribed Oligobrachia species. The new species adds to the cryptic Oligobrachia species complex found at high latitude methane seeps in the north Atlantic and the Arctic. However, this species displays a curled tube morphology and light brown coloration that could serve to distinguish it from other members of the complex. A number of single tentacle individuals were recovered which were initially thought to be members of the only unitentaculate genus, Siboglinum. However, sequencing revealed them to be the new species and the single tentacle morphology, in addition to thin, colorless, and ringless tubes indicate that they are juveniles. This is the first known report of juveniles of northern Oligobrachia. Since the juveniles all appeared to be at about the same developmental stage, it is possible that reproduction is either synchronized within the species, or that despite continuous reproduction, settlement, and growth in the sediment only takes place at specific periods. The new find of the well-known species O. haakonmosbiensis extends its range from the Norwegian Sea to high latitudes of the Arctic in the Fram Strait. We suggest bottom currents serve as the main distribution mechanism for high latitude Oligobrachia species and that water depth constitutes a major dispersal barrier. This explains the lack of overlap between the distributions of northern Oligobrachia species despite exposure to similar current regimes. Our results point toward a single speciation event within the Oligobrachia clade, and we suggest that this occurred in the late Neogene, when topographical changes occurred and exchanges between Arctic and North Atlantic water masses and subsequent thermohaline circulation intensified.

Project description:Marine cold seeps are natural sites of methane emission and harbor distinct microbial communities capable of oxidizing methane. The majority of known cold seeps are on tectonically active continental margins, but recent discoveries have revealed abundant seeps on passive margins as well, including on the U.S. Atlantic Margin (USAM). We sampled in and around four USAM seeps and combined pore water geochemistry measurements with amplicon sequencing of 16S rRNA and mcrA (DNA and RNA) to investigate the microbial communities present, their assembly processes, and how they compare to communities at previously studied sites. We found that the USAM seeps contained communities consistent with the canonical seep microbiome at the class and order levels but differed markedly at the sequence variant level, especially within the anaerobic methanotrophic (ANME) archaea. The ANME populations were highly uneven, with just a few dominant mcrA sequence variants at each seep. Interestingly, the USAM seeps did not form a distinct phylogenetic cluster when compared with other previously described seeps around the world. Consistent with this, we found only a very weak (though statistically significant) distance-decay trend in seep community similarity across a global data set. Ecological assembly indices suggest that the USAM seep communities were assembled primarily deterministically, in contrast to the surrounding nonseep sediments, where stochastic processes dominated. Together, our results suggest that the primary driver of seep microbial community composition is local geochemistry-specifically methane, sulfide, nitrate, acetate, and ammonium concentrations-rather than the geologic context, the composition of nearby seeps, or random events of dispersal. IMPORTANCE Cold seeps are now known to be widespread features of passive continental margins, including the northern U.S. Atlantic Margin (USAM). Methane seepage is expected to intensify at these relatively shallow seeps as bottom waters warm and underlying methane hydrates dissociate. While methanotrophic microbial communities might reduce or prevent methane release, microbial communities on passive margins have rarely been characterized. In this study, we investigated the Bacteria and Archaea at four cold seeps on the northern USAM and found that despite being colocated on the same continental slope, the communities significantly differ by site at the sequence variant level, particularly methane-cycling community members. Differentiation by site was not observed in similarly spaced background sediments, raising interesting questions about the dispersal pathways of cold seep microorganisms. Understanding the genetic makeup of these discrete seafloor ecosystems and how their microbial communities develop will be increasingly important as the climate changes.

Project description:BackgroundMethane seeps support unique benthic ecosystems in the deep sea existing due to chemosynthetic organic matter. In contrast, in shallow waters there is little or no effect of methane seeps on macrofauna. In the present study we focused on the recently described methane discharge area at the northern Laptev Sea shelf. The aim of this work was to describe the shallow-water methane seep macrofauna and to understand whether there are differences in macrobenthic community structure between the methane seep and background areas.MethodsSamples of macrofauna were taken during three expeditions of RV Akademik Mstislav Keldysh in 2015, 2017 and 2018 using 0.1 m2 grabs and the Sigsbee trawl. 21 grabs and two trawls in total were taken at two methane seep sites named Oden and C15, located at depths of 60-70 m. For control, three 0.1 m2 grabs were taken in area without methane seepage.ResultsThe abundance of macrofauna was higher at methane seep stations compared to non-seep sites. Cluster analysis revealed five station groups corresponding to control area, Oden site and C15 site (the latter represented by three groups). Taxa responsible for differences among the station groups were mostly widespread Arctic species that were more abundant in samples from methane seep sites. However, high densities of symbiotrophic siboglinids Oligobrachia sp. were found exclusively at methane seep stations. In addition, several species possibly new to science were found at several methane seep stations, including the gastropod Frigidalvania sp. and the polychaete Ophryotrocha sp. The fauna at control stations was represented only by well-known and widespread Arctic taxa. Higher habitat heterogeneity of the C15 site compared to Oden was indicated by the higher number of station groups revealed by cluster analysis and higher species richness in C15 trawl sample. The development of the described communities at the shallow-water methane seeps can be related to pronounced oligotrophic environment on the northern Siberian shelf.

Project description:In this study we investigated by using 16S rRNA-based methods the distribution and biomass of archaea in samples from (i) sediments above outcropping methane hydrate at Hydrate Ridge (Cascadia margin off Oregon) and (ii) massive microbial mats enclosing carbonate reefs (Crimea area, Black Sea). The archaeal diversity was low in both locations; there were only four (Hydrate Ridge) and five (Black Sea) different phylogenetic clusters of sequences, most of which belonged to the methanotrophic archaea (ANME). ANME group 2 (ANME-2) sequences were the most abundant and diverse sequences at Hydrate Ridge, whereas ANME-1 sequences dominated the Black Sea mats. Other seep-specific sequences belonged to the newly defined group ANME-3 (related to Methanococcoides spp.) and to the Crenarchaeota of marine benthic group B. Quantitative analysis of the samples by fluorescence in situ hybridization (FISH) showed that ANME-1 and ANME-2 co-occurred at the cold seep sites investigated. At Hydrate Ridge the surface sediments were dominated by aggregates consisting of ANME-2 and members of the Desulfosarcina-Desulfococcus branch (DSS) (ANME-2/DSS aggregates), which accounted for >90% of the total cell biomass. The numbers of ANME-1 cells increased strongly with depth; these cells accounted 1% of all single cells at the surface and more than 30% of all single cells (5% of the total cells) in 7- to 10-cm sediment horizons that were directly above layers of gas hydrate. In the Black Sea microbial mats ANME-1 accounted for about 50% of all cells. ANME-2/DSS aggregates occurred in microenvironments within the mat but accounted for only 1% of the total cells. FISH probes for the ANME-2a and ANME-2c subclusters were designed based on a comparative 16S rRNA analysis. In Hydrate Ridge sediments ANME-2a/DSS and ANME-2c/DSS aggregates differed significantly in morphology and abundance. The relative abundance values for these subgroups were remarkably different at Beggiatoa sites (80% ANME-2a, 20% ANME-2c) and Calyptogena sites (20% ANME-2a, 80% ANME-2c), indicating that there was preferential selection of the groups in the two habitats. These variations in the distribution, diversity, and morphology of methanotrophic consortia are discussed with respect to the presence of microbial ecotypes, niche formation, and biogeography.

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Cryptic frenulates are the dominant chemosymbiotrophic fauna at Arctic and high latitude Atlantic cold seeps.

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